Thyroid Endocrine Disruption in Stonerollers and Cricket Frogs from Perchlorate-Contaminated Streams in East-Central Texas

Abstract

In October 2001 and March 2002, a field survey of central stonerollers (Campostoma anomalum) from perchlorate-contaminated streams in central Texas was conducted to assess thyroid endocrine disruption. A survey of adult male and female cricket frogs (Acris crepitans) was performed at the same site between 2001 and 2003. Perchlorate is an oxidizer primarily used in solid-fuel rockets, and many sites that processed or used perchlorate are now contaminated. Histological analysis revealed that the fish from contaminated sites had increased thyroid follicular hyperplasia, hypertrophy, and colloid depletion. Multivariate analysis was generally found to be more powerful than univariate analysis. Seasonal differences existed in the degree of thyroidal perturbation were discovered, and fish were generally less sensitive to thyroidal perturbations in March compared to October. Thyroidal histological indicators were also correlated to levels of perchlorate in the fish, water, and periphyton. Periphyton was frequently most strongly correlated to thyroidal indices, suggesting that exposure through the food chain may be of import. In addition, one of the presumed reference sites turned out to be contaminated with perchlorate, and this was reflected by thyroidal biomarkers before perchlorate was detected in the stream water or biota. There was no evidence of colloid depletion or hyperplasia in frogs from any of the sites, although frogs from two sites with greatest mean water perchlorate concentrations exhibited significantly greater follicle cell hypertrophy. Furthermore, there was a significant positive correlation between follicle cell height and mean water perchlorate concentrations for frogs collected from all sites. This is the first known published account of perchlorate-induced thyroid disruption in fish under field situations, only the second known published account for amphibians, and also points out the value of biomarkers for contaminant biomonitoring.

This is a preview of subscription content, log in to check access.

Figure 1.
Figure 2.
Figure 3.
Figure 4.
Figure 5.
Figure 6.
Figure 7.
Figure 8.
Figure 9.

References

  1. Aas-Hansen O., Johnsen H.K., Vijayan M.M., Jorgensen E.H., (2003). Development of seawater tolerance and concurrent hormonal changes in fed and fasted Arctic charr at two temperature regimes Aquaculture 222: 135–48

    Article  CAS  Google Scholar 

  2. Adams S.M., (2003). Establishing causality between environmental stressors and effects on aquatic ecosystems Hum. Ecol. Risk Assess. 9: 17–35

    Article  CAS  Google Scholar 

  3. Anderson T.A., Wu T.H., (2002). Extraction, cleanup, and analysis of the perchlorate anion in tissue samples Bull. Environ. Contam. Toxicol. 68: 684–91

    Article  CAS  Google Scholar 

  4. Anderson, T.A., Smith P.N., McMurry, S.T., Carr, J.A., Theodorakis, C.W., Jackson, W.A. and Dixon, K.R. (2004). Ecological risk assessment of ammonium perchlorate on fish, amphibian, and mammals in the Lake Belton and Lake Waco watersheds. An integrated laboratory and field investigation. In U.S. Army Corps of Engineers, Bosque and Leon River Watershed Study, Final Report. Fort Worth, TX: U.S. Army Corps of Engineers Fort Worth District

  5. Bhattacharya L., (1995). Histological and histochemical alterations in the thyroid activity of endosulphan treated Oreochromis mossambicus J. Environ. Biol. 16: 347–51

    CAS  Google Scholar 

  6. Bradford, C.M., Carr, J.A., Rinchard, J., and Theodorakis, C. (2005) Perchlorate affects thyroid function in eastern mosquitofish (Gambusia holbrooki) at environmentally relevant concentrations. Eviron. Sci. Technol. 39, 5190-5

    Article  CAS  Google Scholar 

  7. Brown S.B., Adams B.A., Cyr D.G., Eales J.G., (2004a). Contaminant effects on the teleost thyroid Environ. Toxicol. Chem. 23: 1680–701

    Article  CAS  Google Scholar 

  8. Brown S.B., Evans R.E., Vandenbyllardt L., Finnson K.W., Palace V.P., Kane A.S., Yarechewski A.Y., Muir D.C.G., (2004b). Altered thyroid status in lake trout (Salvelinus namaycush). exposed to co-planar 3,3′,4,4′,5-pentachlorobiphenyl Aquat.Toxicol. 67: 75–85

    Article  CAS  Google Scholar 

  9. Burkhead, N.M. (1980). Impact of commercial harvest on stoneroller populations. The life history of the stoneroller minnow Campostoma a. anomalum (Rafinesque) in five streams in east Tennessee. Master’s Thesis, University of Tennessee. Nashville, TN: Tennessee Wildlife Resources Agency

  10. Carr J.A., Urquidi L.J., Goleman W.L., Hu F., Smith P.N., Theodorakis C.W., 2003. Ammonium perchlorate disruption of thyroid function in natural amphibian populations: Assessment and potential impact In: G. Linder, S. Krest, E.E. Little, (eds). Multiple Stressor Effects in Relation to Declining Amphibian Populations. ASTM STP 1443 West Conshohocken, PA ASTM International

    Google Scholar 

  11. Castonguay M., Cyr D.G., (1998). Effects on temperature on spontaneous and thyroxine-stimulated locomotor activity of Atlantic cod J. Fish Biol. 53: 303–13

    Article  CAS  Google Scholar 

  12. Clark J.J., (2000). Toxicology of perchlorate In: Urbansky E.T., (eds). Perchlorate in the Environment New York Kluwer Academic/Plenum Publishers pp 15–29

    Google Scholar 

  13. Cooley H.M., Fisk A.T., Wiens S.C., Tomy G.T., Evans R.E., Muir D.C.G., (2001). Examination of the behavior and liver and thyroid histology of juvenile rainbow trout (Oncorhynchus mykiss). exposed to high dietary concentrations of C sub(10).-, C sub(11).-, C sub(12).- and C sub(14).-polychlorinated n-alkanes Aquat. Toxicol 54: 81–99

    Article  CAS  Google Scholar 

  14. Crouch, N.T. (2003). Investigation of the effects of perchlorate on thyroid and reproductive system function in goldfish. Master’s Thesis. School of Forest Resources, Pennsylvania State University

  15. Cyr D.G., Eales J.G., (1996). Interrelationships between thyroidal and reproductive endocrine systems in fish Rev. Fish Biol. Fisher 6: 165–200

    Article  Google Scholar 

  16. Eales J.G., Brown S.B., (1993). Measurement and regulation of thyroidal status in teleost fish Rev. Fish Biol. Fisher 3: 299–347

    Article  Google Scholar 

  17. Goleman W.L., Carr J.A., Anderson T.A., (2002a). Environmentally relevant concentrations of ammonium perchlorate inhibit thyroid function and alter sex ratios in developing Xenopus laevis Environ. Toxicol. Chem. 21: 424–30

    Article  CAS  Google Scholar 

  18. Goleman W.L., Urquidi L.J., Anderson T.A., Smith E.E., Kendall R.J., Carr J.A., (2002b). Environmentally relevant concentrations of ammonium perchlorate inhibit development and metamorphosis in Xenopus laevis Environ. Toxicol. Chem. 21: 590–7

    Article  CAS  Google Scholar 

  19. Greer M.A., Goodman G., Pleus R.C., Greer S.E., (2002). Health effects assessment for environmental perchlorate contamination, the dose response for inhibition of thyroid radioiodine uptake in human Environ. Health Perspect. 110: 927–37

    CAS  Article  Google Scholar 

  20. Grinwis G.C.M., Besselink H.T., van den Brandhof E.J., Bulder A.S., Engelsma M.Y. Kuiper R.V., Wester P.W., Vaal M.A., Vethaak A.D., Vos J.G., (2000). Toxicity of TCDD in European flounder (Platichthys flesus) with emphasis on histopathology and cytochrome P450 1A induction in several organ systems Aquat. Toxicol. 50:387–401

    Article  CAS  Google Scholar 

  21. Hollander M., Wolfe D.A., (1973). Nonparametric Statistical Methods New York John Wiley & Sons

    Google Scholar 

  22. Howdeshell K.L., (2002). A model of the development of the brain as a construct of the thyroid system Environ. Health Perspect. 110 Suppl 110(suppl 3): 337–48

    CAS  Google Scholar 

  23. Lanno R.P., Dixon D.G., (1994). Chronic toxicity of waterborne thiocyanate to the fathead minnow (Pimephales promelas), a partial life-cycle study Environ. Toxicol. Chem. 13: 1423–32

    Article  CAS  Google Scholar 

  24. Lanno R.P., Dixon D.G., (1996). The comparative chronic toxicity of thiocyanate and cyanide to rainbow trout Aquat. Toxicol. 36: 177–87

    Article  CAS  Google Scholar 

  25. Leatherland J.F., (1994). Reflections on the thyroidoology of fishes, from molecules to Humankind Guelph. Icthyol. Rev. 2: 3–67

    Google Scholar 

  26. MacKenzie D.S., VanPutte C.M., Leiner K.A., (1987). Nutrient regulation of endocrine function in fish Aquaculture 161: 3–25

    Article  Google Scholar 

  27. MacKenzie D.S., Thomas P., Farrar S.M., (1989). Seasonal changes in thyroid and reproductive steroid hormones in female channel catfish (Ictalurus punctatus) in pond culture Aquaculture 78: 63–80

    Article  CAS  Google Scholar 

  28. Manzon R.G., Holmes J.A., Youson J.H., (2001). Variable effects of giotrogens in inducing precocious metamorphosis in sea lampreys (Petromyzon marinus) J. Exp. Zool. 289: 290–303

    Article  CAS  Google Scholar 

  29. Miranda L.A., Paz D.A., Dezi R.E., Pisano A., (1995). Immunocytochemical and morphometric study of TSH, PRL, GH, and ACTH cells in Bufo arenarum larvae with inhibited thyroid function Gen. Comp. Endocrino. 98: 166–76

    Article  CAS  Google Scholar 

  30. Miranda L.A., Pisano A., Paz D.A., (1992). Effect of potassium perchlorate on thyroid activity of Bufo arenarum larvae Comunicaciones Biologicas 10: 125–35

    CAS  Google Scholar 

  31. Motzer W.E., (2001). Perchlorate, problem, detection, and solutions Environ. Forensics 2: 301–11

    Article  CAS  Google Scholar 

  32. Nugegoda D., Wu W., Xu Y., Zhang J., Lichtmannegger J., Schramm K.-W., (2000). Thyroid hormones in fish exposed to PCDD/F and TCDD, from the Yangtze River region, China Organohalogen Compounds 49: 469–73

    CAS  Google Scholar 

  33. Palace V.P., Allen-Gil S.M., Brown S.B., Evans R.E., Metner D.A., Landers D.H., Curtis L.R., Klaverkamp J.F., Baron C.L., Lockhart W.L., (2001). Vitamin and thyroid status in arctic grayling (Thymallus arcticus) exposed to doses of 3,3′,4,4′-tetrachlorobiphenyl that induce the phase I enzyme system Chemosphere 45: 185–93

    Article  CAS  Google Scholar 

  34. Park D., Minor M.D., Propper C.R., (2004). Toxic response of endosulfan to breeding and non-breeding female mosquitofish J. Environ. Biol. 25: 119–24

    CAS  Google Scholar 

  35. Patiño R., Wainscott M.R., Cruz-Li E.I., Balakrishnan S., McMurry C., Blazer V.S., Anderson T.A., (2003). Effects of ammonium perchlorate on the reproductive performance and thyroid condition of zebrafish Environ. Toxicol. Chem. 22: 1115–21

    Article  Google Scholar 

  36. Pavlidis M., Dessypris A., Christofidis I., (1991). Seasonal fuctuations in plasma thyroid hormones, in two strains of rainbow trout (Oncorhynchus mykiss), during the first reproductive and second reproductive cycle – relation with their photoperiodically altered spawning time Aquaculture 99: 65–385

    Article  Google Scholar 

  37. Peter S.M.C., Oommen O.V., (1993). Stiimulation of oxidative-metabolism by thyroid-hormones in propranolol alloxan-treated bony fish, Anabas testudineus (Bloch) J. Exp. Zool. 266: 85–91

    Article  CAS  Google Scholar 

  38. Peter S.M.C., Lock R.A.C., Bonga S.E.W., (2000). Evidence for an osmoregulatory role of thyroid hormones in the freshwater mozambique tilapia Oreochromis mossambicus Gen. Comp. Endocrinol. 120: 157–67

    Article  CAS  Google Scholar 

  39. Power D.M., Llewellyn L., Faustino M., Nowell M.A., Bjoernsson B.Th., Einarsdottir I.E., Canario A.V.M., Sweeney G.E., (2001). Thyroid hormones in growth and development of fish Comp. Biochem. Physiol. C 130: 447–59

    CAS  Google Scholar 

  40. Ram R.N., (1998). Carbofuran-induced histophysiological changes in thyroid of the teleost fish, Channa punctatus (Bloch) Ecotoxicol. Environ. Saf. 16: 106–13

    Article  Google Scholar 

  41. Reddy P.K., Leatherland J.F., (2003). Influences of photoperiod and alternate days of feeding on plasma growth hormone and thyroid hormone levels in juvenile rainbow trout J. Fish Biol. 63: 197–212

    Article  CAS  Google Scholar 

  42. Ricard A.C., Daniel C., Anderson P., Hontela A., (1998). Effects of subchronic exposure to cadmium chloride on endocrine and metabolic functions in rainbow trout Oncorhynchus mykiss Arch. Environ. Contam. Toxicol. 34: 377–81

    Article  CAS  Google Scholar 

  43. Shi Y.B., (2000). Amphibian Metamorphosis: From Morphology to Molecular Biology Wiley-Liss New York, NY, USA

    Google Scholar 

  44. Smith P.N., Theodorakis C.W., Anderson T.A., Kendall R.J., (2001). Preliminary assessment of perchlorate in ecological receptors at the Longhorn Army Ammunition Plant (LHAAP), Karnack, Texas Ecotoxicology 10: 305–13

    Article  CAS  Google Scholar 

  45. Sonstegard R.A., Leatherland J.F., (1984). Great Lakes coho salmon as an indicator organism for ecosystem health Mar. Environ. Res. 14: 480

    Article  Google Scholar 

  46. Sparling D.W., Harvey G., Nzengung V., (2003). Interaction between perchlorates and iodine in the metamorphosis of Hyla versicolor In: G. Linder, S. Krest, E.E. Little, (eds). Multiple Stressor Effects in Relation to Declining Amphibian Populations. ASTM STP 1443 West Conshohocken, PA ASTM International

    Google Scholar 

  47. Stanbury J.B., Wyngaarden J.B., (1952). Effect of perchlorate on the human thyroid gland Metabolism 1: 533–9

    CAS  Google Scholar 

  48. Urbansky E.T., (Eds). (2000). Perchlorate in the Environment New York Kluwer Academic/Plenum Publishers

    Google Scholar 

  49. Urbansky E.T., (2002). Perchlorate as an environmental contaminant Environ. Sci. Pollut. Res. 9: 187–92

    CAS  Article  Google Scholar 

  50. [USACE] U.S. Army Corps of Engineers (2004). Bosque and Leon River Watershed Study, Final Report Fort Worth, TX U.S. Army Corps of Engineers Fort Worth District

    Google Scholar 

  51. Wolff J., (1998). Perchlorate and the thyroid gland Pharmacol. Rev. 50: 89–105

    CAS  Google Scholar 

  52. York R.C., Brown W.R., Girard M.F., Dollarhide J.S., (2001). Two-generation reproduction study of ammonium perchlorate in drinking water in rats evaluates thyroid toxicity Int. J. Toxicol. 20: 183–97

    Article  CAS  Google Scholar 

  53. Zhou T., John-Alder H.B., Weis J.S., Weis P., (1999a). Endocrine disruption: thyroid dysfunction in mummichogs (Fundulus heteroclitus) from a polluted habitat Mar. Environ. Res. 50:393–7

    Article  Google Scholar 

  54. Zhou T., John-Alder H.B., Weis P., Weis J.S., (1999b). Thyroidal status of mummichogs (Fundulus heteroclitus) from a polluted versus a reference habitat Environ. Toxicol. Chem. 18: 2817–23

    Article  CAS  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Christopher W. Theodorakis.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Theodorakis, C.W., Rinchard, J., Carr, J.A. et al. Thyroid Endocrine Disruption in Stonerollers and Cricket Frogs from Perchlorate-Contaminated Streams in East-Central Texas. Ecotoxicology 15, 31–50 (2006). https://doi.org/10.1007/s10646-005-0040-6

Download citation

Keywords

  • Perchlorate
  • Principal Component Analysis Score
  • Perchlorate Concentration
  • Follicle Lumen
  • Cricket Frog